A large superfamily of transmembrane receptors control cellular responses to diverse extracellular signals by catalyzing activation of specific types of heterotrimeric GTP-binding proteins. How these receptors promote nucleotide exchange on G-protein a-subunits to initiate signal amplification is unknown. The three-dimensional structure of the Gt a-subunit C-terminal undecapeptide, Gta(340-350) IKENLKDCGLF, was determined by TRNOE spectroscopy while bound to photoexcited rhodopsin. Light-activation of rhodopsin causes a dramatic shift from a disordered conformation of Gta(340-350) to a binding motif with a helical turn followed by an open reverse turn centered at Gly348, a helix-terminating C-capping motif of an aL-type. Docking of the NMR structure to the GDP-bound X-ray structure of Gt reveals that photoexcited rhodopsin promotes the formation of a continuous helix over residues 325-346 terminated by the C-terminal helical cap with a unique cluster of crucial hydr ophobic si de chains. A molecular mechanism by which activated receptors control G-proteins through reversible conformational changes at the receptor-G protein interface is demonstrated.